ARTIGO ORIGINAL
6
Re is a Cien í ica da O dem dos Médicos www.ac amedicapo uguesa.com
RESUMO
In odução: Os sin omas não-mo o es da doença de Pa kinson são ainda pouco econhecidos, apesa do impac o na qualidade de
ida e na mo alidade. O Ques ioná io de Sin omas Não-Mo o es é uma e amen a álida e con iá el pa a a aliação dos sin omas
não-mo o es nou os idiomas. O obje i o des e es udo é aduzi , adap a e alida a e são po uguesa do Ques ioná io de Sin omas
Não-Mo o es.
Ma e ial e Mé odos: A acei abilidade oi a aliada a a és da ampli ude de alo es, e ei o de e o e de chão. A iabilidade oi medida
em e mos de consis ência in e na (al a de C onbach) e de ep odu ibilidade (coe icien e de co elação in aclasse). Pa a a alidade
de c i é io, o Ques ioná io de Sin omas Não-Mo o es oi compa ado com a escala Mo emen Diso de s Socie y – Uni ied Pa kinson’s
Disease Pa e I. A alidade con e gen e oi a aliada a a és de co elações en e o Ques ioná io de Sin omas Não-Mo o es, Mo e-
men Diso de s Socie y – Uni ied Pa kinson’s Disease Pa e III, pon uação na Mini-Men al S a e Examina ion, du ação de doença e
se e idade de doença.
Resul ados: Rec u ámos 79 doen es com doença de Pa kinson, com idade média de 67,2 ± 10,7 anos e uma du ação média de
doença de 10,8 ± 8,8 anos. A e são po uguesa do Ques ioná io de Sin omas Não-Mo o es e elou p op iedades psicomé icas ade-
quadas. O ques ioná io (al a de C onbach = 0,862) e os seus domínios demons a am uma consis ência in e na adequada, com exce-
ção do domínio ca dio ascula (al a de C onbach = 0,173). Em e mos de alidade, e i ica am-se co elações o es en e a maio ia
dos domínios do Ques ioná io de Sin omas Não-Mo o es e as dimensões co esponden es da Mo emen Diso de s Socie y – Uni ied
Pa kinson’s Disease Pa e I. A pon uação o al do Ques ioná io de Sin omas Não-Mo o es mos ou co elações mode adas com a
du ação e se e idade da doença, se e idade dos sin omas mo o es, não-mo o es e dis unção cogni i a.
Discussão: Es e é o p imei o es udo a aduzi , adap a e alida uma e amen a equen emen e u ilizada pa a as eio de sin omas
não mo o es na doença de Pa kinson.
Conclusão: A e são po uguesa do Ques ioná io de Sin omas Não-Mo o es é uma e amen a álida e con iá el pa a a alia os sin-
omas não-mo o es nos doen es com doença de Pa kinson.
Pala as-cha e: Doença de Pa kinson/diagnós ico; Exame Neu ológico; Inqué i os e Ques ioná ios; Po ugal; Psicome ia; Rep odu-
ibilidade dos Tes es; T adução
T ansla ion, Adap a ion and Valida ion o he Eu opean
Po uguese Ve sion o he NMS-Ques o Pa kinson’s
Disease
T adução, Adap ação e Validação da Ve são Po uguesa
do Ques ioná io de Sin omas Não-Mo o es pa a a
Doença de Pa kinson
1. Neu ology Depa men . Cen o Hospi ala e Uni e si á io de Coimb a. Coimb a. Po ugal.
2. Neu ology Depa men . Faculdade de Medicina. Uni e sidade de Coimb a. Coimb a. Po ugal.
 Au o co esponden e: F adique Mo ei a. [email p o ec ed]
Recebido: 19 de no emb o de 2019 - Acei e: 21 de ab il de 2020 | Copy igh © O dem dos Médicos 2021
Alexand a SILVA1, Tiago PEDRO2, F adique MOREIRA1
Ac a Med Po 2021 Jan;34(1):6-11 ▪ h ps://doi.o g/10.20344/amp.13160
ABSTRACT
In oduc ion: Non-mo o symp oms a e unde ecognized ea u es o Pa kinson’s disease ha impai quali y o li e and inc ease mo a-
li y. In his s udy, we aim o ansla e, adap and alida e he Eu opean Po uguese e sion o he “Non-Mo o Symp oms Ques ionnai e”,
which has p o en o be a alid and eliable measu emen ool o non-mo o symp oms in o he languages.
Ma e ial and Me hods: Accep abili y was e alua ed ega ding he ange o alues, ceiling and loo e ec s. Reliabili y was measu ed
in e ms o in e nal consis ency (C onbach’s alpha) and ep oducibili y (in a-class co ela ion coe icien ). Fo c i e ion alidi y analysis,
Mo emen Diso de s Socie y – Uni ied Pa kinson’s Disease Pa I domains’ sco es we e compa ed o hose o he “Non-Mo o Symp-
oms Ques ionnai e”. Fo con e gen alidi y, co ela ions be ween he “Non-Mo o Symp oms Ques ionnai e” and he Mo emen Diso -
de s Socie y – Uni ied Pa kinson’s Disease Pa III, Mini-Men al S a e Examina ion sco e, disease du a ion, and se e i y we e ob ained.
Resul s: Se en y nine Pa kinson’s disease pa ien s we e ec ui ed, wi h a mean age o 67.2 ± 10.7 yea s and a disease du a ion o
10.8 ± 8.8 yea s. The Eu opean Po uguese e sion o he “Non-Mo o Symp oms Ques ionnai e” o al sco e was ee o signi ican
ceiling and loo e ec s. Wi h he excep ion o he ca dio ascula domain, adequa e o e all in e nal consis ency was achie ed. The
ques ionnai e domains and he co esponding Mo emen Diso de s Socie y – Uni ied Pa kinson’s Disease Pa I dimensions we e
signi ican ly co ela ed, al hough he o al ques ionnai e sco e was modes ly co ela ed wi h disease du a ion and se e i y, mo o and
non-mo o symp oms se e i y and cogni i e dys unc ion.
Discussion: This is he i s s udy o ansla e, adap and alida e a widely used sc eening ins umen o non-mo o symp oms o Eu-
opean Po uguese speaking Pa kinson’s disease pa ien s.
Conclusion: The Eu opean Po uguese e sion o “Non-Mo o Symp oms Ques ionnai e” is a alid and eliable ool o sc eening non-
mo o symp oms in pa ien s wi h Pa kinson’s disease.
Keywo ds: Neu ologic Examina ion; Pa kinson Disease/diagnosis; Po ugal; Psychome ics; Rep oducibili y o Resul s; Su eys and
Ques ionnai es; T ansla ing
Co ec ion/ E a a:
h ps://www.ac amedicapo uguesa.com/ e is a/index.php/amp/a icle/ iew/16510
ARTIGO ORIGINAL
R e i s a C i e n í i c a d a O d e m d o s M é d i c o s w ww. a c a m e d i c a p o u g u e s a . c o m
7
INTRODUCTION
Pa kinson’s disease (PD) is a mul isys em neu ode-
gene a i e diso de , commonly known by i s ca dinal mo-
o ea u es, such as b adykinesia, igidi y, and emo .1
Howe e , non-mo o symp oms (NMS) including cogni i e
impai men , psychia ic, sleep, au onomic, gas oin es inal
and senso y dis u bances a e ound in he majo i y o PD
pa ien s2 and may p ecede he de elopmen o mo o dys-
unc ion.1,3 NMS may ha e a g ea e impac on quali y o
li e han mo o symp oms, wi h se e al s udies showing a
nega i e ou come on he quali y o li e o pa ien s wi h PD.4–7
I s se e i y has been ecen ly shown o inc ease he isk
o mo ali y among Po uguese PD pa ien s.8 Despi e being
highly p e alen and po en ially ea able, hey a e s ill in-
su icien ly diagnosed and emain unde ecognized in o e
50% o he consul a ions pe o med by neu ologis s.9 F e-
quen ly used scales and sco es do no adequa ely de ec
hese non-mo o symp oms,10 which make he de elopmen
o an easy, as and eliable NMS sc eening ool, impe a i e.
The NMS Ques ionnai e (NMS-Ques ) is a sel -comple -
ed pa ien ques ionnai e comp ising 30 quali a i e ques-
ions ha assess he p esence o all impo an non-mo o
symp oms h ough a dicho omic “yes” o “no” answe . The
o iginal English e sion was designed in 2006 o be a quick
sc eening ool used by neu ologis s o pe cei e he pa ien ’s
NMS bu den du ing he p e ious mon h. The ques ionnai e
akes om 10 o 15 minu es o comple e a e which he
i ems can be combined in o nine domains: gas oin es-
inal (8 i ems), u ina y ac (2 i ems), sexual unc ion (2
i ems), ca dio ascula (2 i ems), apa hy/a en ion/memo y
(3 i ems), hallucina ions/delusions (2 i ems), dep ession/
anxie y/anhedonia (2 i ems), sleep/ a igue (5 i ems), pain (1
i em) and miscellaneous (3 i ems).
Since he e is no Po uguese e sion o he NMS-Ques ,
sel - ansla ed e sions a e o en used in clinical p ac ice.
Ou s udy aims o ansla e, adap and alida e he o iginal
NMS-Ques e sion o he Eu opean Po uguese language,
ollowing in e na ional guidelines o adap a ion o ques ion-
nai es.
MATERIAL AND METHODS
Pa icipan s and selec ion
Pa ien s diagnosed acco ding o he Uni ed Kingdom
Pa kinson’s Disease Socie y B ain Bank C i e ia11 we e
consecu i ely ec ui ed om ou Mo emen Diso de s Uni
be ween June and Oc obe 2019. Cogni i e dys unc ion
was sc eened using Mini-Men al S a e E alua ion (MMSE)
and he ollowing cu -o s we e applied: ≤ 15 i illi e a e, ≤
22 i 1 - 11 yea s o educa ion and ≤ 27 i mo e han 11
yea s.12 Cogni i e and debili a ing de ici s (e.g. blindness)
we e es ablished as exclusion c i e ia. Sociodemog aphic
da a we e collec ed ega ding gende , age, and li e acy.
Clinical aspec s including disease du a ion, Hoehn and
Yah (H&Y) scale, Mo emen Diso de s Socie y-Uni ied
Pa kinson’s Disease Ra ing Scale (MDS-UPDRS) – Pa I
and III, and MMSE scale we e e alua ed by he same neu-
ologis . Each ques ionnai e was applied in a p i a e oom
and checked o missing answe s. In o med consen was
ob ained om all pa icipan s and ou p o ocol was ap-
p o ed by he local E hics Commi ee ( e e ence numbe
CHUC-116-19).
NMS-Ques ansla ion and adap a ion
The ansla ion, adap a ion and alida ion p ocess ol-
lowed he ins uc ions p o ided by he Mo emen Diso -
de s Socie y upon eques and he s udy was conduc ed
acco ding o he Good Clinical P ac ice guidelines.13 The
o iginal English e sion o NMS-Ques was i s ansla ed
in o Po uguese by wo independen bilingual expe s and
a consensual e sion was ob ained a e g amma ical and
seman ic compa ison. Then, he consensus e sion was
back- ansla ed in o English by ano he bilingual speake
unawa e o he o iginal scale o ule ou seman ic disc ep-
ancies be ween he o iginal and he ansla ed e sion o
he scale. The Po uguese e sion o NMS-Ques was e-
iewed by an expe ienced clinician and highly knowledge-
able in Mo emen Diso de s o es o con en alidi y, and
i was applied in a p e es ing ial wi h 10 PD pa ien s in
o de o assess cul u al di e ences and sensi i i ies. A inal
Po uguese e sion o NMS-Ques was c ea ed a e wa ds
and is p esen ed in Appendix 1 (see Appendix 1: h ps://
www.ac amedicapo uguesa.com/ e is a/index.php/amp/
a icle/ iew/13160/Appendix_01.pd ).
Da a analysis
Desc ip i e s a is ics we e used o sample demog aph-
ic cha ac e iza ion and ques ionnai e esul s. Con en alid-
i y was achie ed h ough expe e iew. Fo analysis pu -
poses, he i ems we e g ouped in o nine domains ollowing
he ecommenda ions o he Mo emen Diso de s Socie y:
diges i e (i ems 1 o 7), u ina y (i ems 8 and 9), apa hy/
a en ion/memo y (i ems 12, 13, and 15), hallucina ions/
delusions (i ems 14 and 30), dep ession/anxie y (i ems 16
and 17), sexual unc ion (i ems 18 and 19), ca dio ascula
(i ems 20 and 21), sleep diso de s (i ems 22 o 26), and
miscellany (i ems 10, 11, 27, 28, and 29). One poin was
sco ed in case o a posi i e answe o each ques ion and
ze o poin s in case o a nega i e esponse. The inal sco e
o each domain was hen calcula ed and pa ien s wi h a
leas one posi i e answe we e conside ed o ha e co e-
sponding symp oms o ha domain.
Fo con e gen alidi y, co ela ions be ween NMS-
Ques domains and MDS-UPDRS Pa III, MMSE sco es,
and disease du a ion and se e i y we e pe o med using
he Spea man co ela ion coe icien (ρ). Co ela ions we e
conside ed e y s ong when a coe icien was g ea e han
0.90, s ong i be ween 0.70 and 0.90, mode a e i be ween
0.50 and 0.70, weak i be ween 0.30 and 0.50 and e y
weak i below 0.30.14 C i e ion alidi y was analyzed by
co ela ing NMS-Ques and MDS-UPDRS Pa I domains
sco es using Spea man co ela ion coe icien (ρ). Some
MDS-UPDRS Pa I i ems we e g ouped in o a common di-
mension compa able o ha in he NMS-Ques , al hough
Sil a A, e al. Po uguese e sion o he NMS-Ques o Pa kinson’s disease, Ac a Med Po 2021 Jan;34(1):6-11
ARTIGO ORIGINAL
8
Re is a Cien í ica da O dem dos Médicos www.ac amedicapo uguesa.com
sexual unc ion (NMS-Ques ) and dopamine dys egula ion
synd ome (MDS-UPDRS Pa I) we e le wi hou possible
compa ison. The accep abili y was e alua ed in e ms o
ange o alues, ceiling and loo e ec s. An e ec ≤ 15% is
conside ed accep able. In e nal consis ency o each domain
was es ed using C onbach’s alpha and alues ≥ 0.70 we e
conside ed adequa e indica o s o eliabili y. The es - e es
and in a- a e eliabili y we e assessed using in a-class
co ela ion (ICC) based on an absolu e-ag eemen , 2-way
mixed-e ec s model. A coe icien ≥ 0.70 was deemed as
accep able.14
The s a is ical analysis was execu ed using IBM SPSS
e sion 25 wi h a le el o signi icance se a 0.05.
RESULTS
A o al o 79 PD pa ien s we e included, he majo i y o
which we e males (57%; n = 45). The pa icipan s had a
mean age o 67.2 ± 10.7 yea s ( ange 35 - 87) and a mean
disease du a ion o 10.8 ± 8.8 yea s. The mean H&Y s age
was 2.3 ± 0.6 (3.8%, n = 3 in s age 1; 67.1%, n = 53 in
s age 2; 25.3%, n = 20 in s age 3; 3.8%, n = 3 in s age 4).
The MDS-UPDRS-Pa III mean sco e o mo o symp oms
se e i y was 30.7 ± 13.0 and he MDS-UPDRS-Pa I mean
sco e o non-mo o symp oms se e i y was 10.5 ± 4.9. The
clinical and demog aphic ea u es a e shown in Table 1.
Accep abili y
As shown in Table 2, gas oin es inal symp oms we e
he mos common and we e epo ed by 82.3% (n = 65)
o pa ien s, ollowed by sleep diso de s (81.0%; n = 64).
Hallucina ions and/o delusions we e p esen in 27.8% (n
= 22) o pa ien s and we e he leas equen . All domains
showed a loo e ec , wi h hallucina ions/delusions being
he mos p ominen (72.2%). Apa om he diges i e and
miscellany domains, all o he s showed a ceiling e ec , he
highes (68.4%) being p esen ed by he dep ession/anxie y
dimension. The NMS-Ques o al sco e was ee o signi i-
can ceiling (2.5%) and loo (1.3%) e ec s.
Reliabili y
Ou Po uguese e sion o he NMS-Ques exhibi ed an
o e all C onbach’s alpha o 0.862 and an ICC o 0.848. Fo
each domain, he alpha coe icien s anged om 0.183 o
0.902. Excep o he ca dio ascula domain (0.183), he
diges i e (0.764), u ina y (0.840), apa hy/a en ion/memo y
(0.803), hallucina ions/delusions (0.885), dep ession/anxi-
e y (0.874), sexual unc ion (0.902), sleep diso de s (0.810)
and miscellaneous symp oms (0.730) we e ound o be
in e nally consis en . The o e all esul s o he ICC we e
equi alen , indica ing sa is ac o y es - e es eliabili y.
Validi y
C i e ion alidi y analysis is shown in Table 3. All NMS-
Ques and ela ed MDS-UPDRS-Pa I domains we e posi-
i ely co ela ed wi h a signi icance alue below 0.001. The
co ela ion coe icien s anged om 0.361 (miscellaneous
symp oms) o 0.911 (hallucina ions/delusions). S ong co -
ela ions we e ob ained be ween he diges i e, u ina y, apa-
hy/a en ion/memo y, dep ession/anxie y, ca dio ascula
Sil a A, e al. Po uguese e sion o he NMS-Ques o Pa kinson’s disease, Ac a Med Po 2021 Jan;34(1):6-11
Table 1 – S udy sample cha ac e is ics
Fea u es
Age (yea s)*67.2 ± 10.7
Gende , M/F (%M) 45/34 (57)
Yea s o educa ion*6.7 ± 4.3
Disease du a ion*10.8 ± 8.8
H&Y s age, % (n)
13.8 (3)
267.1 (53)
325.3 (20)
43.8 (3)
MMSE sco e*27.3 ± 2.7
MDS-UPDRS-Pa I sco e*10.5 ± 4.9
MDS-UPDRS-Pa III sco e*30.7 ± 13.0
* Values a e mean ± s anda d de ia ion
H&Y: Hoehn & Yah scale; MDS-UPDRS: Mo emen Diso de s Socie y - Uni ied Pa kin-
son’s Disease Ra ing Scale; MMSE: Mini-Men al S a e Examina ion
Table 2 – Desc ip i e analysis and psychome ic indica o s o NMS-Ques domains
NMS-Ques domain
Accep abili y Reliabili y
% (n) Range Mean ± SD Ceiling
e ec , %
Floo
e ec , % ICC C onbach’s
alpha
Diges i e 82.3 (65) 0.0 - 7.0 2.7 ± 2.1 1.3 17.7 0.741 0.764
U ina y 72.2 (57) 0.0 - 2.0 1.3 ± 0.9 59.5 27.8 0.839 0.840
Apa hy/A en ion/Memo y 74.7 (59) 0.0 - 3.0 1.8 ± 1.2 43.0 25.3 0.798 0.803
Hallucina ions/ Delusions 27.8 (22) 0.0 - 2.0 0.5 ± 0.8 20.3 72.2 0.885 0.885
Dep ession/Anxie y 77.2 (61) 0.0 - 2.0 1.5 ± 0.8 68.4 22.8 0.876 0.874
Sexual unc ion 62.0 (49) 0.0 - 2.0 1.2 ± 0.9 53.2 38.0 0.902 0.902
Ca dio ascula 70.9 (56) 0.0 - 2.0 0.9 ± 0.7 24.1 29.1 0.173 0.183
Sleep diso de s 81.0 (64) 0.0 - 5.0 2.4 ± 1.9 21.5 19.0 0.804 0.810
Miscellany 67.1 (53) 0.0 - 5.0 1.6 ± 1.6 8.9 32.9 0.729 0.730
To al - 2.0 - 28.0 13.7 ± 6.3 2.5 1.3 0.848 0.862
ICC: in aclass co ela ion coe icien ; SD: s anda d de ia ion
ARTIGO ORIGINAL
R e i s a C i e n í i c a d a O d e m d o s M é d i c o s w ww. a c a m e d i c a p o u g u e s a . c o m
9
Sil a A, e al. Po uguese e sion o he NMS-Ques o Pa kinson’s disease, Ac a Med Po 2021 Jan;34(1):6-11
and sleep diso de s domains and hei co esponding MDS-
UPDRS-Pa I dimensions. The equency o hallucina-
ions and/o delusions in he NMS-Ques p esen ed a e y
s ong co ela ion wi h he hallucina ions/psychosis i em in
he MDS-UPDRS-Pa I, while he equency o miscellane-
ous symp oms was weakly co ela ed wi h pain and o he
sensa ions on he espec i e scales. The e we e no logical
ma ches o he NMS-Ques sexual domain and he dopa-
mine dys egula ion synd ome in he MDS-UPDRS-Pa I.
Cons uc alidi y was assessed compa ing he NMS-
Ques domain sco es wi h clinical indica o s. The co ela ion
ma ix is shown in Table 4. The majo i y o he NMS-Ques
dimensions p esen ed a weak o mode a e co ela ion wi h
he MDS-UPDRS-Pa I sco e, excep o he sexual unc-
ion domain. The domains conce ning diges i e, ca dio-
ascula and sleep diso de s exhibi ed e y-weak o weak
co ela ions wi h mo o symp oms se e i y (MDS-UPDRS-
Pa III sco e). Rega ding cogni i e unc ion, he diges i e,
apa hy/a en ion/memo y, hallucina ions/delusions, and de-
p ession/anxie y domains we e nega i ely co ela ed wi h
he MMSE sco e. Howe e , he sexual unc ion domain was
posi i ely co ela ed wi h a highe cogni i e s a us.
Only domains conce ning hallucina ions/delusions and
sleep diso de s showed posi i e and e y weak o weak
co ela ions wi h disease du a ion. In e ms o disease se-
e i y, he diges i e, u ina y, ca dio ascula , sleep diso de s
and miscellany domains we e posi i ely co ela ed wi h he
H&Y s age. These co ela ions we e conside ed e y weak
o weak.
DISCUSSION
Ou s udy is he i s Eu opean Po uguese ansla ion
and adap a ion o he o iginal English e sion o he NMS-
Ques ha ollows he in e na ional equi emen s o scale
alida ion. Gi en hei high p e alence and bu den, we p o-
ide a eliable and alid sc eening ins umen o non-mo o
symp oms in PD. The NMS-Ques di e s om all o he non-
mo o symp oms ques ionnai es due o i s sel -comple ed
and quali a i e na u e. I can be easily illed ou by pa ien s
du ing o e en be o e consul a ions. I allows us o o e -
come some o he ime es ain s du ing ollow-up consul-
a ions and he pa ien s’ emba assmen in epo ing hei
symp oms.
Table 3 – Spea man co ela ion coe icien s (ρ) be ween NMS-Ques and MDS-UPDRS-Pa I dimensions
NMS-Ques domain MDS-UPDRS-Pa I domain ρ*
Diges i e 1.11 Cons ipa ion p oblems 0.767
U ina y 1.10 U ina y p oblems 0.750
Apa hy/A en ion/Memo y 1.1 Cogni i e impai men
1.5 Apa hy 0.813
Hallucina ions/Delusions 1.2 Hallucina ions, psychosis 0.911
Dep ession/Anxie y 1.3 Dep essed mood
1.4 Anxious mood 0.752
Sexual unc ion -
Ca dio ascula 1.12 Ligh headedness 0.822
Sleep diso de s
1.7 Sleep p oblems
1.8 Day ime sleepiness
1.13 Fa igue
0.784
Miscellany 1.9 Pain and o he sensa ions 0.361
-1.6 Dopamine dys egula ion synd ome -
MDS-UPDRS: Mo emen Diso de s Socie y Uni ied Pa kinson’s Disease Ra ing Scale
*All co ela ion coe icien s we e signi ican a p < 0.001.
Table 4 – Spea man co ela ion coe icien s (ρ) be ween NMS-Ques dimensions and o he applied scales o disease s ages
NMS-Ques domain MDS-UPDRS-Pa I MDS-UPDRS-Pa III MMSE Disease du a ion H&Y s age
Diges i e 0.569*0.492*-0.244*0.181 0.354*
U ina y 0.352*0.193 -0.091 -0.099 0.233*
Apa hy/A en ion/Memo y
0.613*0.111 -0.223*0.081 0.197
Hallucina ions/Delusions 0.344*0.167 -0.241*0.297*0.116
Dep ession/Anxie y 0.540*0.220 -0.326*-0.057 0.211
Sexual unc ion 0.058 -0.077 0.329*0.102 -0.007
Ca dio ascula 0.520*0.263*-0.169 0.076 0.358*
Sleep diso de s 0.537*0.373*-0.163 0.302*0.441*
Miscellany 0.462*0.087 -0.064 0.126 0.250*
*p < 0.05
H&Y: Hoehn & Yah scale; MDS-UPDRS: Mo emen Diso de s Socie y - Uni ied Pa kinson’s Disease Ra ing Scale; MMSE: Mini-Men al S a e Examina ion
ARTIGO ORIGINAL
10
Re is a Cien í ica da O dem dos Médicos www.ac amedicapo uguesa.com
The Po uguese NMS-Ques showed adequa e psycho-
me ic p ope ies in he ields o accep abili y, eliabili y, and
alidi y. The o e all sco e did no show any ceiling and loo
e ec s, al hough hey we e p esen in mos o he domains
ha con ained a small numbe o i ems due o he inc eased
likelihood o sco ing he highes and lowes possible on
hose i ems. The ca dio ascula NMS-Ques domain did
no each accep able in e nal consis ency and es - e es
eliabili y in ou s udy. This domain is composed o one i em
sc eening o dizziness seconda y o o hos a ic hypo en-
sion and ano he ega ding he equency o alls. Al hough
o hos a ic hypo ension may indeed p omp pa ien s o all,
mo o complica ions (pos u al ins abili y, gai eezing, dys-
kinesias) ha e been es ablished as majo isk ac o s o
alling,15–17 which may explain he low in e nal consis ency
coe icien ob ained.
O he NMS-Ques domains such as gas oin es inal and
miscellaneous symp oms showed only ma ginally accep -
able in e nal consis ency. The gas oin es inal domain in-
cludes one i em conce ning cons ipa ion while also sc een-
ing o in es inal incon inence. Al hough bo h can be p esen
a he same ime, we ound ha obs ipa ion was epo ed
by 58.2% o pa ien s and in es inal incon inence by 8.9%,
which is consis en wi h p e ious s udies18,19 bu e lec ed
on a lowe C onbach’s alpha coe icien . Only i e pa ien s
epo ed hese symp oms simul aneously and had a longe
disease du a ion when compa ed wi h he o e all sample
(mean 17.2 yea s). Mo eo e , he miscellany domain is
composed o i ems ha canno i in any o he o he ca ego-
ies. The e o e, i is expec ed ha hese symp oms a e no
consis en ly p esen among pa ien s wi h PD.
Signi ican co ela ions be ween all NMS-Ques do-
mains and he co esponding i ems on he MDS-UPDRS-
Pa I we e ound. Hallucina ions and/o delusions showed
he s onges associa ion wi h he ma ching i em on ou
‘gold-s anda d’ scale, bu he miscellaneous clus e showed
a weak co ela ion p obably due o concep ual di e ences.
The miscellany domain in he NMS-Ques comp ises i ems
es ing o pain, weigh changes, swelling, swea ing and
diplopia while he co esponding MDS-UPDRS-Pa I i em
only men ions pain, ingling, and c amps.
Rega ding cons uc alidi y, we we e able o es ablish
signi ican co ela ions be ween each NMS-Ques domain
and disease- ela ed a iables (MDS-UPDRS-Pa I, MDS-
UPDRS-Pa III, MMSE, disease du a ion, and H&Y s age).
Diges i e and ca dio ascula symp oms p esen ed he
s onges co ela ions wi h disease se e i y, bu no wi h
disease du a ion, which is in line wi h B aak’s pa hological
indings whe e he degene a ion o he au onomic ne ous
sys em and lowe b ain s em p ecedes ha o he co ex as
he disease sp eads.20 The se e i y o mo o symp oms was
mainly co ela ed wi h he p esence o diges i e symp oms.
These symp oms may an icipa e he mo o mani es a ions
o he disease, and pa icula ly dysphagia, cons ipa ion,
and ecal incon inence can be caused o wo sened by gas-
oin es inal muscles dysmo ili y.21
In e es ingly, sexual unc ion was he only domain exhib-
i ing a posi i e co ela ion wi h he MMSE sco e, indica ing
ha sexual pe o mance was highly dependen on cogni-
i e s a us. This e ec has been epo ed in men, whe e de-
c eased cogni i e unc ion was associa ed wi h less sexual
in e es and loss o libido.22
The e is a lack o compa able da a wi h o he NMS-
Ques alida ion s udies. To ou knowledge, only he I alian
ansla ion and alida ion23 ollowed a simila me hodology,
bu he di e ences in he g ouping o he i ems p e en ed us
om d awing di ec compa isons. When compa ed wi h he
o iginal scale alida ion coho ,24 ou pa ien s had a highe
disease du a ion (10.8 ± 8.8 s 6.4 ± 4.3 yea s), lowe dis-
ease se e i y (2.3 ± 0.6 s 2.5) and we e sligh ly younge
(67.2 ± 10.7 s 68.1 ± 10.3 yea s old). These ac s could
explain he epidemiological di e ences be ween he e-
quency o non-mo o symp oms obse ed and ha epo ed
on he o iginal scale alida ion and gene al s udies. While
me a-analyses show ha u ina y p oblems a e he mos
p e alen among PD pa ien s a ound he wo ld,25 sleep/
a igue, and ca dio ascula symp oms we e epo ed o be
he mos equen in he Po uguese popula ion.26
The e a e limi a ions o ou s udy wo h men ioning.
Fi s , ou sample was also smalle compa ed o ha o he
o iginal scale alida ion (79 s 123 pa ien s), bu simila
o o he ansla ions and alida ions.23,27 The majo i y o
he pa ien s had mild o mode a e s ages o he disease,
which may unde es ima e he epo ing o symp oms ypi-
cal o ad anced s ages (memo y loss, apa hy, dep ession,
e c.)28 and in luence he gene alizabili y o he esul s. Fu-
u e s udies conce ning he applicabili y o he NMS-Ques
in ad anced s ages o he disease a e equi ed. Also, ou
‘gold-s anda d’ scale (MDS-UPDRS-Pa I) does no include
i ems enqui ing o sexual dys unc ion symp oms ha could
be used o he alidi y analysis o he sexual unc ion do-
main o he NMS-Ques . Finally, he g ouping o con a y o
un ela ed symp oms may ha e led o he low in e nal con-
sis ency and c i e ion alidi y obse ed in some domains,
espec i ely.
CONCLUSION
The Po uguese e sion o he NMS-Ques is a use ul
sc eening ool o non-mo o symp oms in PD pa ien s ha
mee s he alidi y and eliabili y equi emen s in he majo i y
o i s domains. Ca dio ascula and gas oin es inal sco es
should be in e p e ed ca e ully. We ecommend he ou ine
use o NMS-Ques in he ou pa ien se ing o help diagnose
and ea iden i ied symp oms.
ACKNOWLEDGMENTS
We hank Joana Lopes and Sónia Sac amen o o hei
help du ing ansla ion and pa ien ec ui men .
PROTECTION OF HUMANS AND ANIMALS
The au ho s decla e ha he p ocedu es we e ollowed
acco ding o he egula ions es ablished by he Clinical Re-
sea ch and E hics Commi ee and o he Helsinki Decla a-
ion o he Wo ld Medical Associa ion.
Sil a A, e al. Po uguese e sion o he NMS-Ques o Pa kinson’s disease, Ac a Med Po 2021 Jan;34(1):6-11

ARTIGO ORIGINAL
R e i s a C i e n í i c a d a O d e m d o s M é d i c o s w ww. a c a m e d i c a p o u g u e s a . c o m
11
Sil a A, e al. Po uguese e sion o he NMS-Ques o Pa kinson’s disease, Ac a Med Po 2021 Jan;34(1):6-11
DATA CONFIDENTIALITY
The au ho s decla e ha ing ollowed he p o ocols in
use a hei wo king cen e ega ding pa ien s’ da a publica-
ion.
CONFLICTS OF INTEREST
The au ho s epo no con lic s o in e es .
FUNDING SOURCES
This esea ch ecei ed no speci ic g an om any und-
ing agency in he public, comme cial, o no - o -p o i sec-
o s.
REFERENCES
1. Kalia LV, Lang AE. Pa kinson’s disease. Lance . 2015;386:896–912.
2. Zhang TM, Yu SY, Guo P, Du Y, Hu Y, Piao YS, e al. Nonmo o symp oms
in pa ien s wi h Pa kinson disease: a c oss-sec ional obse a ional
s udy. Medicine. 2016;95:e5400.
3. Chaudhu i KR, Healy DG, Schapi a AH. Non-mo o symp oms o
Pa kinson’s disease: diagnosis and managemen . Lance Neu ol.
2006;5:235–45.
4. Be ganzo K, Tije o B, Gonzalez-Eizagui e A, Somme J, Lezcano
E, Gabilondo I, e al. Mo o and non-mo o symp oms o Pa kinson’s
disease and hei impac on quali y o li e and on di e en clinical
subg oups. Neu ologia. 2016;31:585–91.
5. McNeely ME, Duncan RP, Ea ha GM. Impac s o dance on non-mo o
symp oms, pa icipa ion, and quali y o li e in Pa kinson disease and
heal hy olde adul s. Ma u i as. 2015;82:336–41.
6. Es ada-Bellmann I, Cama a-Lema oy CR, Calde on-He nandez HJ,
Rocha-Anaya JJ, Villa eal-Velazquez HJ. Non-mo o symp oms and
quali y o li e in pa ien s wi h Pa kinson’s disease in No heas e n
Mexico. Ac a Neu ol Belg. 2016;116:157–61.
7. Palme i R, Lo Buono V, Bonanno L, So be a C, Cimino V, B aman i P, e
al. Po en ial p edic o s o quali y o li e in Pa kinson’s disease: sleep and
mood diso de s. J Clin Neu osci. 2019;70:113–7.
8. Bugalho P, Ladei a F, Ba bosa R, Ma o JP, Bo binha C, Sala isa M, e
al. Mo o and non-mo o unc ion p edic o s o mo ali y in Pa kinson’s
disease. J Neu al T ansm. 2019;126:1409–15.
9. Shulman LM, Taback RL, Rabins ein AA, Weine WJ. Non- ecogni ion
o dep ession and o he non-mo o symp oms in Pa kinson’s disease.
Pa kinsonism Rela Diso d. 2002;8:193–7.
10. S o ch A, Odin P, T ende -Ge ha d I, Fuchs G, Rei schneide G,
Chaudhu i KR, e al. Non-mo o symp oms ques ionnai e and scale
o Pa kinson’s disease. C oss-cul u al adap a ion in o he Ge man
language. Ne ena z . 2010;81:980–5.
11. Va ney S, Lockha I, Bakhshi L, Richa ds A, Ingham J, Klaeijsen E.
Pa kinson’s disease: na ional clinical guideline o diagnosis and
managemen in p ima y and seconda y ca e. NICE Clinical Guidelines.
2011;1:10022.
12. San ana I, Du o D, Lemos R, Cos a V, Pe ei a M, Simões MR, e al. Mini-
men al s a e examina ion: a aliação dos no os dados no ma i os no
as eio e diagnós ico do dé ice cogni i o. Ac a Med Po . 2016;29:240–
8.
13. G imes DA, Hubache D, Nanda K, Schulz KF, Mohe D, Al man DG.
The good clinical p ac ice guideline: a b onze s anda d o clinical
esea ch. Lance . 2005;366:172–4.
14. Te wee CB, Bo SD, de Boe MR, an de Wind DA, Knol DL, Dekke
J, e al. Quali y c i e ia we e p oposed o measu emen p ope ies o
heal h s a us ques ionnai es. J Clin Epidemiol. 2007;60:34–42.
15. Fa ombi TH, Owolabi MO, Ogunniyi A. Falls and hei associa ed isks in
Pa kinson’s disease pa ien s in Nige ia. J Mo Diso d. 2016;9:160–5.
16. Wood BH, Bilclough JA, Bow on A, Walke RW. Incidence and p edic ion
o alls in Pa kinson’s disease: a p ospec i e mul idisciplina y s udy. J
Neu ol Neu osu g Psychia y. 2002;72:721–5.
17. G ay P, Hildeb and K. Fall isk ac o s in Pa kinson’s disease. J Neu osci
Nu s. 2000;32:222–8.
18. Edwa ds LL, P ei e RF, Quigley EM, Ho man R, Ballu M.
Gas oin es inal symp oms in Pa kinson’s disease. Mo Diso d.
1991;6:151–6.
19. Sakakiba a R, Kishi M, Ogawa E, Ta eno F, Uchiyama T, Yamamo o T,
e al. Bladde , bowel, and sexual dys unc ion in Pa kinson’s disease.
Pa kinsons Dis. 2011;2011: 924605.
20. B aak H, T edici KD, Rüb U, de Vos RA, Jansen S eu EN, B aak E.
S aging o b ain pa hology ela ed o spo adic Pa kinson’s disease.
Neu obiol Aging. 2003;24:197–211.
21. Ce sosimo MG, Bena och EE. Neu al con ol o he gas oin es inal
ac : implica ions o Pa kinson disease. Mo Diso d. 2008;23:1065–75.
22. Kumme A, Ca doso F, Teixei a AL. Loss o libido in Pa kinson’s disease.
J Sex Med. 2009;6:1024–31.
23. Co a I, Di Ba is a ME, Vanaco e N, Papi CP, Alampi G, Rubino A, e
al. Adap a ion and psychome ic p ope ies o he I alian e sion o he
non-mo o symp oms ques ionnai e o Pa kinson’s disease. Neu ol Sci.
2017;38:673–8.
24. Chaudhu i KR, Ma inez-Ma in P, Schapi a AH, S occhi F, Se hi K, Odin
P, e al. In e na ional mul icen e pilo s udy o he i s comp ehensi e
sel -comple ed nonmo o symp oms ques ionnai e o Pa kinson’s
disease: he NMSQues s udy. Mo Diso d. 2006;21:916–23.
25. Taglia i M, Chaudhu i K, Pagano G. P e alence o non-mo o symp oms
in Pa kinson’s disease:a sys ema ic e iew wi h me a-analysis.
Neu ology. 2014;82:P2.053.
26. Bugalho P, Lamp eia T, Miguel R, Mendonça MD, Cae ano A, Ba bosa
R. Non-mo o symp oms in Po uguese Pa kinson’s sisease pa ien s:
co ela ion and impac on quali y o li e and ac i i ies o daily li ing. Sci
Rep. 2016;6:1–9.
27. Rios Romene s S, Wol son C, Gala as C, Pelle ie A, Al man R, Wadup
L, e al. Valida ion o he non-mo o symp oms ques ionnai e (NMS-
Ques ). Pa kinsonism Rela Diso d. 2012;18:54–8.
28. Tan ee K, A ique I, Sadiq W, Ahmad A. Non-mo o symp oms in
pa ien s wi h Pa kinson’s disease: a c oss-sec ional su ey. Cu eus.
2018;10:e3412.